Adaptive mutations: a challenge to neo-Darwinism?

Abstract

Introduction During the last decade microbial geneticists have become intrigued with an extremely unorthodox phenomenon, i.e. the capacity of certain mutations to occur more often when the resulting phenotype is more advantageous for the cell. increased mutational rates and different mutation profiles, relative to those observed in bacteria grown under non-selective conditions, have been observed after prolonged incubation on nutritionally depleted solid surfaces. Such mutational events have been described as adaptive, directed, Cairnsian, or selection-induced. phenomenon is strongly reminiscent of the Lamarckian view of evolution, and consequently, it is in sharp contrast to the basic tenet of neo-Darwinism that mutations are random events unrelated to any immediate utility. Quite understandingly, the original paper The Origin of Mutants by Cairns et al. (1) was followed by a flurry of comments, but also soon by reports confirming the original findings in other systems. A large body of data has been accumulated on adaptive mutations in the meantime. In this paper, I focus on the most typical examples obtained on Eschericia coli which has been the experimental system for the most of the studies. For more interested readers I recommend two excellent, more extensive reviews. more critical paper by Lenski and Muller (2) on one side, and the rather pro tinted paper by Foster (3) on the other, offer an optimal combination of material for personal judgment. Classical experiments on bacterial mutations world of Prokariota was the last to which Mendelian concepts of gene and the notion of gene mutation, were extended. reason for this and the long time lag in the development of bacterial genetics, stemmed from the mere nature of microorganisms. Namely, in higher organisms the experimenters were able to observe mutations and their phenotypes in individual plants and animals even when most of such mutations would have been counterselective to their bearers outside the laboratory. In contrast, the character differences observed in bacterial variations always referred to population. Bacteriologists could neither observe individual mutants nor infer their existence without applying selection. Even such basic characteristics as the colour or morphology of a bacterial colony might not have been the consequence of the original mutant cell, but rather the representation of the few million ceils that make up a visible colony. In another words, it was impossible to decide whether observed variations were the consequence of preferential growth of the original (pre-existing) mutant or the result of adaptive mass conversion of the whole population under particular selection. answer to the problem came in 1943 when Luria and Delbruck devised the fluctuation test (Figure 1) (4). experimental model was based on the well known phenomenon of the occasional appearance of E. coli mutants resistant to the virulent phage T1 ([Ton.sup.r] mutants). experiment was designed to decide between two fundamentally opposed views: (1), resistance of E. coli to T1 phage is induced as the consequence of the attach of phage on sensitive bacteria. More precisely, each bacterium in the population has a small chance to become resistant upon contact with phage. resistance is the result of the descendants. (2) [Ton.sup.r] character is generated by stochastic mutational events independently of the phase. It pre-exists in the small subpopulation of bacteria and it is only selected in the present of the phage. Under the first hypothesis, which is strongly reminiscent of the Lamarckian view of the evolutionary processes, the number of [Ton.sup.r] clones on the plates seeded with aliquots of bacteria from parallel cultures and the excess of T1 phage, should be approximately the same, whereas under the second neo-Darwinian hypothesis, the number of [Ton.sup.r] mutants should vary significantly due to the temporal randomness of the mutational events; the earlier the mutation occurs in the growing cultures, the larger the population of [Ton. …